EFFECTS OF ACUTE FATIGUE ON THE VOLITIONAL AND

MAGNETICALLY-EVOKED ELECTROMECHANICAL DELAY OF THE

KNEE FLEXORS IN MALES AND FEMALES

1Claire Minshull ( ), 2Nigel Gleeson, 3Michelle Walters-Edwards, 2Roger Eston and

4David Rees

1School of Biomedical and Natural Sciences, Nottingham Trent University, Nottingham, UK, NG11 8NS; 2School of Sport and Health Sciences, St Luke’s Campus, University of Exeter, Exeter, UK, EX1 2LU; 3School of Health Professions, Marymount University, Arlington, USA; 4National Centre for Sports Injury Surgery, RJAH Orthopaedic Hospital, Shropshire, UK, SY10 7AG.

Correspondence address:

Dr. Claire Minshull,

School of Biomedical and Natural Sciences,

Clifton Campus, Nottingham Trent University,

Nottingham, U.K., NG11 8NS

Tel.: +44 (0)115 8483205

Fax: +44 (0)115 8486636

e-mail: claire.minshull@ntu.ac.uk

1

Abstract

Neuromuscular performance capabilities, including those measured by evoked responses,

may be adversely affected by fatigue; however, the capability of the neuromuscular

system to initiate muscle force rapidly under these circumstances is yet to be established.

Sex-differences in the acute responses of neuromuscular performance to exercise stress

may be linked to evidence that females are much more vulnerable to ACL injury than

males. Optimal functioning of the knee flexors is paramount to the dynamic stabilisation

of the knee joint, therefore the aim of this investigation was to examine the effects of

acute maximal intensity fatiguing exercise on the voluntary and magnetically-evoked

electromechanical delay in the knee flexors of males and females. Knee flexor volitional

and magnetically-evoked neuromuscular performance was assessed in seven male and

nine females prior to and immediately after: (i) an intervention condition comprising a

fatigue trial of 30-seconds maximal static exercise of the knee flexors, (ii) a control

condition consisting of no exercise. The results showed that the fatigue intervention was

associated with a substantive reduction in volitional peak force (PFV) that was greater in

males compared to females (15.0%, 10.2%, respectively, p < 0.01) and impairment to

volitional electromechanical delay (EMDV) in females exclusively (19.3%, p < 0.05).

Similar improvements in magnetically-evoked electromechanical delay in males and

females following fatigue (21%, p < 0.001), however, may suggest a vital facilitatory

mechanism to overcome the effects of impaired voluntary capabilities, and a faster

neuromuscular response that can be deployed during critical times to protect the joint

system.

Keywords: Fatigue, neuromuscular performance, electromechanical delay, magnetic

stimulation

2

Introduction

During strenuous activities, mechanical loading of the knee joint can often exceed the

tensile capacities of the passive structures (Johansson et al. 1991). As a consequence,

greater reliance may be placed on the protective capabilities of the surrounding

musculature in order to maintain joint integrity (Gleeson et al. 1998a). Evidence of

anterior cruciate ligament (ACL) injury by means of non-contact mechanisms in team

sports athletes (Ireland et al. 1997; Mandelbaum et al. 2005; Rees 2004) underscores the

potentially important contribution of neuromuscular mechanisms to the maintenance of

dynamic joint stability and the avoidance of injury. As evidence shows that females are

five to eight times more likely to injure their ACL compared to male counterparts given

equivalent exposure to sport (Arendt and Dick, 1995; Ireland et al. 1997; Gray et al.

1985), study of factors that might affect the stability of the knee joint in females is

important.

Optimal functioning of the knee flexors in particular is considered fundamental to

the prevention of ACL injury (Gleeson and Mercer 1996; Johansson et al. 1991; Rees

1994), however, a limited time frame exists whereby potentially harmful dynamic forces

must be overcome by the most rapid response of the neuromuscular system in order to

protect ligamentous tissue against injury (Gleeson et al. 1998a; Huston and Wojtys 1996;

Mercer et al. 1998; Shultz et al. 2001). For the ACL, the time frame from the initial

application of such forces to the complete rupture of the ligament has been estimated at

300 ms (Rees, 1994). One aspect of the overall neuromuscular reaction time has been

defined as electromechanical delay (EMD). It depicts the time between the onset of

electrical activity and the onset of tension in skeletal muscle (Zhou et al. 1996) and is

3

associated with the propagation of the action potential through the muscle and the

stretching of the series elastic component (Norman & Komi, 1979). It represents an

important aspect of neuromuscular reaction time, during which there could be

unrestrained development of forces of sufficient magnitude to damage ligamentous tissue

in synovial joints (Gleeson et al. 2000; Huston and Wojtys 1996; Mercer et al. 1998;

Shultz et al. 2001). The importance of this index of performance can be exemplified

further by recognising that factors such as muscle fatigue can cause increases in EMD

latency of up to 70% (Zhou et al. 1996). The extent of this change in EMD performance

may also be influenced by the loading of viscoelastic structures, which can cause creep

within the affected tissue and a modulation of the neuromuscular performance

characteristics of the associated musculature (Chu et al. 2003; Sbriccoli et al, 2005;

Solomonow, 2004; Solomonow et al. 2003). Clearly, any fatigue-related increases in

muscle response time within the knee flexors to initiate force, coupled with the effects of

increased ligamentous laxity and compliance within muscle-related connective tissue

associated with cyclical loading during activity, may result in a hyper-lax system that is

more likely to be incapable of restraining high joint loads rapidly enough to prevent

ligamentous injury.

Traditionally, neuromuscular performance capabilities have been estimated

routinely in the laboratory by means of assessment protocols involving volitional

activation of muscle. Recent technological advances, however, have enabled the non-

invasive and painless magnetic stimulation of a peripheral motor nerve; the efficacy of

this technique has been considered in clinical populations where maximal volitional

testing is not appropriate (Polkey et al. 1996; Vivodtzev et al. 2005). Peripheral magnetic

stimulation of a nerve root offers the potential to activate the fastest motor units (King

4

and Chippa 1989; Maertens de Noordhout 1991) and overcome factors associated with

the volitional activation of muscle that might otherwise intrude on the proper estimation

of an individual’s true maximal performance capacity. For example, factors such as

autogenic neuromuscular inhibition associated with injury and conditioning status might

tend to elicit an underestimation of performance capability even in the most highly

motivated of individuals (Gleeson 2001; Hopkins and Ingersoll 2000). A corollary of this

interpretation is that assessments of neuromuscular performance by means of magnetic

stimulation may offer greater insights into the performance capability that might be

available to the sports performer in emergency situations where there is a critical level of

threat to the stability of the joint system.

Acute muscle fatigue induced by means of maximal voluntary muscle activation

(MVMA) has the potential to cause dramatic increases in EMD; of between 42% to 70%

longer compared with pre-fatigue values (Horita and Ishiko 1987;, Zhou et al. 1996) and

concomitant decreases in the capacity for generating peak force. Temporal impairments

of this type to the dynamic muscle stabilisers of the knee joint, may affect the ability to

stabilise the knee during competitive match-play and place the sports performer at

increased risk of injury. Studies of fatigue-related changes to EMD measured using

electrically-evoked activation of muscle, however, have yielded conflicting findings of

impaired (Zhou 1996), unchanged (Strojnik and Komi 1998) and even improved

performance (Sahlin and Seger 1995). Given the potential inhibitory effects on

performance that pain may elicit under conditions of electrical stimulation, an evoked

assessment of the neuromuscular system by means of magnetic stimulation, a technique

that minimises intrusion of noxious stimuli, may offer a truer insight into the maximal

5

physiological capacity for rapid muscle activation. No studies have yet investigated the

effects of acute muscle fatigue on the magnetically-evoked EMD of the knee flexors.

The aim of this investigation was to examine the effects of an acute bout of

maximal intensity static fatiguing exercise on the voluntary and magnetically-evoked

electromechanical delay in the knee flexors of males and females.

6

Methods

Subjects

Seven men (age: 29.6 (± 10.4) yrs; height 1.78 (± 0.04) m; body mass 77.0 (± 7.7) kg

(mean [± SD]) and nine women (age 25.2 (± 4.2) yrs; height 1.69 (± 0.08) m; body mass

62.8 (± 8.1) kg) gave their informed consent to participate in this study. All participants

were regularly involved in exercise (at least 3 times per week) and were asymptomatic at

the time of assessment. Participants were instructed to refrain from strenuous physical

activity for the 24 hours prior to the test. Assessment protocols were approved by the

Ethics Committee for Human Testing of the University of Wales, Bangor.

Experimental procedures

Following habituation procedures, participants completed a standardised warm-up of five

minutes cycle ergometry (90 watts for males, 60 watts for females) and a further five

minutes of static stretching of the involved musculature. This warm-up was equivalent to

that used in other recent studies within this laboratory examining the effects of various

interventions on indices of volitional neuromuscular performance (Gleeson 2001;

Gleeson et al. 2000; Gleeson et al. 1998a; Gleeson et al. 1998b; Mercer et al. 1998).

Participants were then secured in a prone position on a custom-built dynamometer

(Gleeson et al. 1995).

The experimental design comprised two treatment conditions: (i) an intervention

condition that required participants to perform a fatigue trial of 30 seconds maximal static

fatiguing exercise of the knee flexors of the preferred leg; (ii) a control condition of

equivalent duration to the intervention consisting of no exercise. Treatment conditions

were separated by twenty minutes. The control condition was performed first in order to

7

avoid any potential carry-over effects. Participants were verbally encouraged during

periods of maximal muscle activation. Estimates of knee flexor volitional and

magnetically-evoked neuromuscular performance were obtained prior to and immediately

after each treatment condition. The protocol is illustrated schematically in figure 1.

Participant and dynamometer orientation

Participants were secured in a prone position on the dynamometer. The bi-lateral lever-

arms of the dynamometer were attached to the legs of the participant by means of padded

ankle-cuffs and adjustable strapping just proximal to the lateral malleolus. The

dynamometer’s and knee joint’s axes of rotation were aligned as closely as possible.

Figure 1. A schematic of the protocol to assess the effects of an acute fatiguing task on the volitional and magnetically-evoked neuromuscular performance of the knee flexors.

Adjustable strapping across the mid-thoracic spine, pelvis and posterior thigh proximal to

the knee localised the action of the involved musculature. A functionally relevant knee

flexion angle of 25 degrees (0.44 rad) associated with the greatest mechanical strain on key

ligaments (Beynnon and Johnson 1996), was maintained throughout testing. This angle

was identified for each participant during activation of the involved musculature using a

goniometer system. Once secured into position and prior to testing, participants were

required to perform a series of warm-up muscle activations, comprising of 2 x 25%, 50%,

8

75% and 100% of subjectively-judged maximal voluntary peak force. Each of the

activations was sustained for three seconds and was separated from the next by 10 seconds.

The orientation of the participant and dynamometer is illustrated schematically in figure 1.

Assessment of neuromuscular performance

Maximal volitional muscle activation (MVMA)

On receipt of an auditory signal, given randomly within 1-4 seconds, the participants

attempted to activate their musculature as rapidly and forcefully as possible by attempting

to flex the knee joint against the immovable restraint offered by the apparatus. Another

auditory signal was given to the participant after 2 - 3 seconds of MVMA to cue

neuromuscular relaxation. Intra-trial MVMA replicates were each separated by at least 10

seconds to enable neuromuscular recovery (Moore and Kukulka 1991).

Magnetically-evoked muscle activation

Supra-maximal magnetic stimulation of the sciatic nerve (L4-L5) and associated activation

of the knee flexors was achieved by means of double wound coil (120 mm) that was

powered by a Magstim 200 stimulator (Magstim Co. Ltd., Whitland, Dyfed, Wales). The

optimum site for stimulation of the nerve was defined as the site that offered the largest

amplitude of the compound muscle action potential (CMAP). This was identified by a

procedure in which the centre of the magnetic coil was placed in a position 20 mm to 40

mm lateral to the fifth lumbar vertebra on the involved side and then small iterative

positional changes of the coil were made that were commensurate with increasing CMAP

responses during a series of discrete stimulations. This optimised coil position was

maintained manually throughout the remainder of the test.

9

There appears to be no standardised way described in the literature that

systematically verifies the attainment of supra-maximal magnetic stimulation of a

peripheral motor nerve. Protocols to elicit supra-maximal stimulation of the femoral nerve

have been described briefly in the literature (Polkey et al. 1996; Vivodtzev et al. 2005).

However, these protocols have been limited to the verification of a supra-maximal

response by changes in peak twitch force data only due to the intrusion of stimulation

artefact compromising the quality of muscle EMG recordings. As such, CMAP amplitude

responses have not previously been used in a verification process. A protocol was

developed for the current study in which supra-maximal stimulation was defined as the

intensity of stimulation at which there was subsequently no more than a 5% increase in

CMAP peak amplitude despite a 10% or greater increase in the intensity of stimulation,

and verified using a procedure that would mimic the approach to the physiological

verification of the attainment of maximal oxygen uptake. Thus supra-maximal stimulation

was verified by contemporaneous visual inspection of the data during a sequence of seven

discrete stimulations of increasing intensity that commenced at 40% of the Magstim 200’s

maximal capacity output with subsequent increments of 10% to 100% of capacity.

Retrospective analyses of CMAP amplitude and peak twitch force demonstrated

proportionate and linear increases when plotted against one another. In the four

participants from the present study whose CMAP amplitude did not by definition reach

supra-maximal proportions, supplementary criteria that were based on minimal

simultaneous increases in the performance of peak twitch force (PTFE) and

electromechanical delay (< 5% increase in performance elicited by stimulations of

increasing intensity between 80% and 100% of the Magstim 200’s maximal capacity

output) were used to verify that ‘peak’ amplitudes of CMAP had occurred (Minshull et al.

2002a; Minshull et al. 2002b). The latter instances were associated with limitations of the

10

technological capability of the stimulation system. Sequential stimulations throughout the

experimental period were separated by at least 10 seconds to ensure neuromuscular

recovery (Moore and Kukulka 1991).

Indices of neuromuscular performance

Peak force

Volitional static peak force (PFV) was recorded as the mean response of three intra-trial

replicates in which the highest force was recorded in each trial. Compensation procedures

for gravitational errors in forces recorded in the vertical plane were undertaken

immediately prior to testing.

Electromechanical delay

Electromyographic activity (EMG) was recorded from the m. biceps femoris during the

estimation of PFV and subsequent to supra-maximal stimulation. The EMG was recorded

using bipolar surface electrodes (self-adhesive, silver-silver chloride, 10 mm diameter) that

were applied longitudinally over the belly of m. biceps femoris, on the line between the

ischial tuberosity and the lateral epicondyle of the femur. The m. biceps femoris was

selected as an important contributor to restraint of anterior tibio-femoral displacement and

lateral rotation of the femur relative to the tibia since both processes have been implicated

in ACL injury (Fu et al. 1993).

The raw unfiltered EMG signals was passed through a differential amplifier, input

impedance 10,000 MOhms , CMMR 100 dB, and a gain of 1000 (Cambridge Electronic

Design,UK). The signal, which incorporated minimal intrusion from induced currents

associated with external electrical and electromagnetic sources and noise inherent in the

11

remainder of the recording instrumentation, was analogue-to-digitally converted at 2.5 kHz

sample rate, ensuring a significant margin of reserve between the highest frequency

expected in the EMG signal and the Nyquist frequency and minimal intrusion from

aliasing errors (Gleeson, 2001). The EMG signals remained unfiltered during subsequent

analyses. The inter-electrode distance was 30 mm and a reference electrode was placed 30

mm lateral and equidistant from the recording electrodes. Standardised skin preparation

techniques yielded inter-electrode impedance of less than 5 kΩ.

Volitional and magnetically-evoked EMD (EMDV and EMDE, respectively) were

computed as the mean response of three intra-trial muscle activations in which the time

delay between the onset of electrical activity and the onset of force was recorded. Post-

fatigue EMDE was estimated on the basis of performance in a single trial to minimise the

potential intrusion of neuromuscular recovery on recorded scores. The superior

reproducibility (coefficient of variation expressed as a percentage of the mean group score)

and single measurement reliability (intra-class correlation coefficient) characteristics

associated with EMDE compared to the equivalent volitional estimates of performance

have been described previously (8.1%; 0.84 vs. 10.1%; 0.80 for EMDE and EMDV,

respectively) (Minshull et al. 2002b). The onset of electrical activity was defined as the

first point in time at which the electrical signal exceeded consistently the 95% confidence

limits of the isoelectric line associated with the background electrical noise amplitude and

quiescent muscle, and which was the first deviation of the recorded electrical signal that

was congruent with physiological activation of the muscle. Onset of muscle force was

defined as the first point in time at which the force record exceeded consistently the 95%

confidence limits associated with the electrical noise amplitude of the load cells (see

figures 2 and 3). Onset of muscle force was defined as the first point in time at which the

12

force record exceeded consistently the 95% confidence limits associated with the electrical

noise amplitude of the load cells (see figures 2 and 3).

Figure 2. Example raw data showing: upper trace: example data of force and EMG associated with one MVMA; lower trace: magnification of muscle activation to show representative calculation of volitional electromechanical delay (EMDV).

Figure 3. Example data showing; upper trace: example data of force and EMG associated with a single magnetic stimulus; lower trace: magnification of muscle activation to show representative calculation of magnetically-evoked electromechanical delay (EMDE).

13

Statistical analysis

The effect of the fatiguing exercise intervention was assessed for each index of

performance (PFV; EMDV; EMDE) using separate two (condition: control; fatigue) by two

(time: pre; post) by two (group: male; female) mixed-model ANOVAs with repeated

measures on the first two factors. The assumptions underpinning the use of repeated

measures ANOVA were checked and violations corrected by the Greenhouse-Geisser

adjustment of the critical F-value, as indicated by GG. Statistical significance was

accepted at p < 0.05.

The experimental design offered an approximate .80 power of avoiding a Type-II

error when employing a least detectable difference of 16 N, 8 ms and 3.5 ms for PFV,

EMDV and EMDE, respectively.

14

Results

Volitional muscle activation

Volitional peak force (PFV)

A significant three-factor interaction showed that while absolute strength performance

was preserved during the control task, the fatiguing exercise task elicited a reduction in

absolute strength performance in both males and females (F[1,14] = 14.0, p < 0.05).

However, the absolute strength performance (group mean score (± SD)) was impaired to

a greater extent in males than in females compared to baseline scores (265.1 (± 52.0) N

vs. 311.8 (± 52.8) N [15% impairment] and 171.4 (± 33.9) N vs. 190.8 (± 48.6) N [10.2%

impairment], respectively).

Figure 4. The effects of the fatigue task on the volitional peak force (PFV) of the knee flexors (group mean ± SD).

Electromechanical delay (EMDV)

A significant three-factor interaction (F[1,14] = 5.9, p < 0.05) suggested that EMDV

performance was maintained during the control task for both groups and in the

15

experimental condition for males. However, the fatiguing exercise task elicited a 19.5%

impairment in EMDV performance compared to baseline levels in females (61.2 (± 19.0)

ms vs. 51.2 (± 13.1) ms, respectively) (see figure 5). A-priori Helmert contrasts between

group mean scores for males and females at baseline revealed no significant differences

in EMDV performance.

Figure 5. The effects of the fatigue task on the volitional electromechanical delay (EMDV) of the knee flexors (group mean ± SD).

Magnetically-evoked muscle activation

Evoked electromechanical delay (EMDE)

A significant two-factor interaction of condition (control; fatigue) by time (pre; post) on

EMDE showed that while absolute EMDE performance was preserved during the control

task, the fatiguing exercise task elicited a potentiation (21% decrease) in EMDE latencies

in both males and females (F[1,14] = 27.3, p < 0.001) (see figure 6). A-priori Helmert

contrasts between males and females at baseline revealed significantly shorter absolute

EMDE values in females compared to males (F[1,14] = 7.3, p < 0.05)

16

Figure 6. The effects of the fatigue task on the magnetically-evoked electromechanical delay (EMDE) of

the knee flexors (group mean ± SD).

17

Discussion

The absence of change over the control condition for each index of performance indicates

that there were no systematic or learning effects and that performance variation can be

attributed to the exercise intervention.

Volitional neuromuscular performance

The exercise intervention induced fatigue in the knee flexors, characterised by a

significant decrease in PFV from pre- to post-fatiguing exercise levels. The magnitude of

PFV performance decrement observed in the current study (15% for males and 10% for

females) is congruent with the extent of performance loss associated with match play in

team games such as soccer (Gleeson et al. 1998b). These findings, together with

corroborating findings from other studies (e.g. Gleeson et al. 2000; Gleeson et al. 1998b;

Zhou et al. 1996) may suggest a reduced capability of the dynamic stabilisers to provide

forceful corrective responses to mechanical loading of the knee. Such fatigue-related

changes in neuromuscular performance may be interpreted to represent an increased risk

of injury (Chan et al. 2001; Gleeson et al. 1998b; Mercer et al. 1998), which may be

amplified particularly at knee angles where key ligamentous structures are already under

greatest mechanical strain (Beynnon and Johnson 1996).

Recent research has demonstrated that loading of viscoelastic structures in

isolation can cause creep within the affected tissue and a modulation of the

neuromuscular performance characteristics of the associated musculature (Chu et al.

2003; Sbriccoli et al. 2005; Solomonow, 2004; Solomnow et al. 2003). For example,

cyclical loading (150-200N) of the anterior cruciate ligament has been associated with an

18

approximate 10% reduction in knee extensor peak force (Sbriccoli et al, 2005).

Furthermore, outcomes of testing in animal models have reported increases in shear creep

of up to 27% and 53% respectively, compared to baseline following ten minutes and

thirty minutes of intermittent bouts of feline spinal flexion (Solomnow et al. 2003).

Sporting pursuits involving cyclical loading of viscoelastic tissue may contribute to

increased injury risk because compliance characteristics and reflexive muscular activity

may be adversely affected (Solomonow, 2004). However, the magnitude of the loading

applied cyclically on viscoelastic tissue within the present study was probably low. For

example, the loading effect of gravity in the current study would have created a relatively

small passive anterior shear force on the knee of approximately 10-15N. This force is

likely to have been moderated further by the frequent periods of muscle activation

performed by participants, shielding relevant tissue from mechanical stress. It is likely

that the cyclical application of such forces will have contributed an effect to baseline

performance by means of the duration of the standardised warm-up (5 minutes of cyclical

loading) and a small effect to the experimental changes in EMD performance following

the acute 30 second fatigue-task, plus time spent in static maximal voluntary muscle

actions.

While the decrements to PFV capabilities of males exceeded that experienced by

females (PFV: 15% vs. 10%, respectively), a group mean increase in EMDV latencies from

pre- to post-fatigue levels (19.3%) was observed exclusively in females. Recent research

that has indicated that the reaction time of the neuromuscular system to imposed dynamic

forces may be fundamental to the protection of the joint system (Gleeson et al. 2000;

Gleeson et al. 1998a; Gleeson et al. 1998b; Huston and Wojtys 1996; Mercer et al. 1998;

Shultz et al. 2001) may suggest such concomitant increases in EMDV may affect the timely

19

correction of joint forces and be associated with exacerbation of injury risk. Indeed, the

current results may provide a new insight into the complex phenomenon that describes a

five- to seven-fold increase risk of ACL injury in the female athlete compared to male

counterparts (Gray et al. 1985; Ireland et al. 1997).

The processes involved in the conversion of excitation into muscle force can

potentially contribute to the fatigue-related changes in the force-generating capability

observed in the current study. However, it has been proposed that the majority of the

EMD is determined by the time taken to stretch the series elastic component (SEC)

(Cavanagh and Komi 1979), most of which is situated at the connective tissue

attachments at the end of the muscle fibres (McComas 1996). The differential changes in

EMDV performance between sexes in the current study could be partially explained by a

generally greater compliance in biologic tissue in females (Wojtys et al. 1998),

exacerbated by muscle temperature increases associated with the fatiguing exercise (Zhou

et al. 1998). Given the many injury risk factors experienced by females, habituated

exposure to scenarios where knee joint stability may be under threat might condition the

neuromuscular system of the healthy female athlete at functional joint angles. The

subsequent formation of pre-programmed responses that provide fast compensatory

reactions to joint perturbations (Latash 1998) may quickly harness the SEC and account

for the parity in EMDV performance observed between the sexes at baseline. Under

conditions of muscle fatigue and sustained loading, however, this capability may be

diminished due to a reduction of the effectiveness of the fastest most powerful motor

units, impairing the temporal capability of the muscle to ‘gather in’ a more compliant

SEC.

20

Magnetically-evoked neuromuscular performance

Despite the fatiguing exercise intervention causing fatigue and impairment to indices of

volitional neuromuscular performance, the ultimate temporal physiological capacity of

the neuromuscular system (EMDE), as measured by magnetic stimulation, was potentiated

by similar amounts in both males and females.

Our understanding of aspects of the nature of fatigue may be challenged

somewhat by the observed differences in fatigue-related changes to EMDV and EMDE.

However, the apparent paradoxical coexistence of fatigue of volitional performance and

potentiation of evoked performance has been documented previously subsequent to

exercise. Improvements of electrically-evoked peak twitch force (Rassier and MacIntosh

2000) and EMD (Sahlin and Seger 1995) have been described following acute and

prolonged exercise protocols, respectively. It is plausible that these changes facilitate a

biological conservation of resources during energy-costly volitional exercise efforts,

while simultaneously offering enhanced reflex and ‘emergency’ capabilities to resist

mechanical threats to musculoskeletal integrity. While metabolically mediated increases

in sensitivity of muscle contractile proteins to Ca2+ may represent the processes

underlying potentiated muscle force characteristics (Rassier and MacIntosh 2000),

exercise-related changes to the compliance characteristics of the musculoskeletal system

may represent the principal potentiating processes in the present study. This may be

particularly true considering that the major proportion of EMD is accounted for by

lengthening of the SEC (Komi 1979; Zhou et al. 1995).

Connective tissue and muscle-tendon units subjected to a constant stress elongate

over time (stress-relaxation), eliciting an increased length at a given load (Stone and

21

Karatzaferi 1992). Recently, this creep effect has been shown to elicit a ‘disordering’ of

the neuromuscular reflex response and, coupled with the concomitant increase in

connective tissue compliance and ligamentous laxity, has been interpreted as representing

a major knee injury risk factor (Chu et al. 2003; Solomonow, 2004). In is interesting to

note that results from the current investigation, show an improvement in magnetically-

evoked EMD following fatigue. This shortening of evoked latency may suggest that the

exercise-related stress and assessment characteristics elicited a decrease in compliance

within the knee joint system. It is conceivable that the strong static activation of muscle

induced reactive hyperemia (McComas 1996) and a potential distension of the muscle.

These latter processes may have contributed substantially to the facilitated post-fatigue

EMDE when coupled with comparably reduced levels of muscle force that would be

required to stretch stress-relaxed viscoelestic structures.

The implications of the potentiation of EMDE performance may be commensurate

with the potential to overcome the fatigue-related impairments of the volitional

performance capabilities during critical times. The net result following acute volitional

muscle fatigue may be a ‘reserve capacity’ of unused motor units that can be deployed

during perceived threat to the joint system. The utility of this preserved emergency

capacity to the individual athlete may be dependent entirely, however, on the down-

regulation of these potential protective central and peripheral neuromuscular inhibitory

mechanisms (Hopkins and Ingersoll 2000) that appear to limit access to the full capacity

of large high threshold motor units under voluntary conditions (Tsuji and Nakamura

1988; Zhou et al. 1995). This inhibition may be exemplified by the longer latencies

associated with EMDV (e.g. 51.2 ms) compared to EMDE (e.g. 27.0 ms) in this study. A

further corollary of this interpretation suggests that methods of assessment of

22

performance capacity must be carefully considered, since utilisation of solely volitional

means of assessment may predispose a gross underestimation of the true capacity of the

neuromuscular system.

In summary, the substantive decrement to the force-generating capacity of the

knee flexors in males and females following acute fatigue (10% and 15% decreases in

PFV, respectively) may demonstrate a reduced capability to provide adequate dynamic

restraint in response to mechanical loading of the knee joint at functional joint angles. In

addition, the significant increase of EMDV in females following acute muscle fatigue

(19%) may be congruent with a reduced temporal capability to harness stabilising or

resistive forces at the knee and place the female sports performer at increased risk of

injury compared to male counterparts. Potentiation of magnetically-evoked EMD

following fatigue in both males and females may suggest a capability to overcome the

effects of impaired voluntary neuromuscular performance. Yet, the efficacy of a

preserved temporal performance capacity to avoid synovial joint injury may be dependent

entirely on whether the neuromuscular recruitment strategies observed subsequent to

magnetic stimulation can be replicated under non-evoked conditions. Ultimately,

increased risk of injury is likely to reflect the complex interaction of several factors, some

of which may include neuromuscular conditioning, susceptibility to fatigue and an ability

to deploy the full motor unit capacity of the neuromuscular system at crucial times.

Acknowledgements

The authors wish to acknowledge the help of the School of Sport, Health and Exercise,

University of Wales, Bangor, where the data for this study was originally collected.

23

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